Structural organization of the spongy mesophyll

Borsuk, Aleca M.; Roddy, Adam B.; Théroux‐Rancourt, Guillaume; Brodersen, Craig R.

doi:10.1111/nph.17971

Title: Structural organization of the spongy mesophyll

Journal Article · 14 February 2022 · New Phytologist

DOI: https://doi.org/10.1111/nph.17971 · OSTI ID:1845156

^[1];

^[2];

^[3];

^[1]

School of the Environment Yale University New Haven CT 06511 USA
Department of Biological Sciences Institute of Environment Florida International University Miami FL 33199 USA
Department of Integrative Biology and Biodiversity Research Institute of Botany University of Natural Resources and Life Sciences, Vienna 1180 Vienna Austria

Summary Many plant leaves have two layers of photosynthetic tissue: the palisade and spongy mesophyll. Whereas palisade mesophyll consists of tightly packed columnar cells, the structure of spongy mesophyll is not well characterized and often treated as a random assemblage of irregularly shaped cells. Using micro‐computed tomography imaging, topological analysis, and a comparative physiological framework, we examined the structure of the spongy mesophyll in 40 species from 30 genera with laminar leaves and reticulate venation. A spectrum of spongy mesophyll diversity encompassed two dominant phenotypes: first, an ordered, honeycomblike tissue structure that emerged from the spatial coordination of multilobed cells, conforming to the physical principles of Euler’s law; and second, a less‐ordered, isotropic network of cells. Phenotypic variation was associated with transitions in cell size, cell packing density, mesophyll surface‐area‐to‐volume ratio, vein density, and maximum photosynthetic rate. These results show that simple principles may govern the organization and scaling of the spongy mesophyll in many plants and demonstrate the presence of structural patterns associated with leaf function. This improved understanding of mesophyll anatomy provides new opportunities for spatially explicit analyses of leaf development, physiology, and biomechanics.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1845156

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 234; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (85)

The correlation between cell division and the shapes and sizes of prismatic cells in the epidermis of cucumis Lewis, Frederic T. The Anatomical Record, Vol. 38, Issue 3 https://doi.org/10.1002/ar.1090380305	journal	May 1928
A comparison between the mosaic of polygons in a film of artificial emulsion and the pattern of simple epithelium in surface view (cucumber epidermis and human amnion) Lewis, Frederic T. The Anatomical Record, Vol. 50, Issue 3 https://doi.org/10.1002/ar.1090500303	journal	September 1931
Structure and mechanics of the iris leaf Gibson, L. J.; Ashby, M. F.; Easterling, K. E. Journal of Materials Science, Vol. 23, Issue 9 https://doi.org/10.1007/BF00551271	journal	September 1988
The Honeycomb Conjecture Hales, T. C. Discrete & Computational Geometry, Vol. 25, Issue 1 https://doi.org/10.1007/s004540010071	journal	January 2001
Evaluation of photosynthetic electron flow using simultaneous measurements of gas exchange and chlorophyll fluorescence under photorespiratory conditions Ye, Z. P.; Yu, Q.; Kang, H. J. Photosynthetica, Vol. 50, Issue 3 https://doi.org/10.1007/s11099-012-0051-5	journal	September 2012
Foliar, Physiologial and Growth Responses of Four Maple Species Exposed to Ozone Calatayud, Vicent; Cerveró, Júlia; Sanz, María José Water, Air, and Soil Pollution, Vol. 185, Issue 1-4 https://doi.org/10.1007/s11270-007-9446-5	journal	July 2007
Hexagonal territories Barlow, George W. Animal Behaviour, Vol. 22 https://doi.org/10.1016/0003-3472(74)90010-4	journal	November 1974
Some remarks on the arrangement of grains in a polycrystal Weaire, D. Metallography, Vol. 7, Issue 2 https://doi.org/10.1016/0026-0800(74)90004-4	journal	April 1974
Accumulation of the phytoalexin lettucenin a and changes in 3-hydroxy-3-methylglutaryl coenzyme a reductase activity in lettuce seedlings with the red spot disorder Bestwick, L.; Bennett, M. H.; Mansfield, J. W. Phytochemistry, Vol. 39, Issue 4 https://doi.org/10.1016/0031-9422(95)00089-P	journal	July 1995
Controls on gross production by a semiarid forest growing near its warm and dry ecotonal limit Fellows, Aaron W.; Goulden, Michael L. Agricultural and Forest Meteorology, Vol. 169 https://doi.org/10.1016/j.agrformet.2012.10.001	journal	February 2013
BoneJ: Free and extensible bone image analysis in ImageJ Doube, Michael; Kłosowski, Michał M.; Arganda-Carreras, Ignacio Bone, Vol. 47, Issue 6 https://doi.org/10.1016/j.bone.2010.08.023	journal	December 2010
Bioinspired engineering of honeycomb structure – Using nature to inspire human innovation Zhang, Qiancheng; Yang, Xiaohu; Li, Peng Progress in Materials Science, Vol. 74 https://doi.org/10.1016/j.pmatsci.2015.05.001	journal	October 2015
Embracing 3D Complexity in Leaf Carbon–Water Exchange Earles, J. Mason; Buckley, Thomas N.; Brodersen, Craig R. Trends in Plant Science, Vol. 24, Issue 1 https://doi.org/10.1016/j.tplants.2018.09.005	journal	January 2019
Photosynthesis Optimized across Land Plant Phylogeny Gago, Jorge; Carriquí, Marc; Nadal, Miquel Trends in Plant Science, Vol. 24, Issue 10 https://doi.org/10.1016/j.tplants.2019.07.002	journal	October 2019
A 4000-species dataset provides new insight into the evolution of ferns Testo, Weston; Sundue, Michael Molecular Phylogenetics and Evolution, Vol. 105 https://doi.org/10.1016/j.ympev.2016.09.003	journal	December 2016
Equilibrium bicontinuous structure Scriven, L. E. Nature, Vol. 263, Issue 5573 https://doi.org/10.1038/263123a0	journal	September 1976
The global spectrum of plant form and function Díaz, Sandra; Kattge, Jens; Cornelissen, Johannes H. C. Nature, Vol. 529, Issue 7585 https://doi.org/10.1038/nature16489	journal	December 2015
Developmentally based scaling of leaf venation architecture explains global ecological patterns Sack, Lawren; Scoffoni, Christine; McKown, Athena D. Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1835	journal	January 2012
A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution de Boer, Hugo Jan; Eppinga, Maarten B.; Wassen, Martin J. Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2217	journal	January 2012
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Hydraulic basis for the evolution of photosynthetic productivity Scoffoni, Christine; Chatelet, David S.; Pasquet-kok, Jessica Nature Plants, Vol. 2, Issue 6 https://doi.org/10.1038/nplants.2016.72	journal	May 2016
Mesophyll porosity is modulated by the presence of functional stomata Lundgren, Marjorie R.; Mathers, Andrew; Baillie, Alice L. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10826-5	journal	June 2019
Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana Kaiser, Elias; Morales, Alejandro; Harbinson, Jeremy Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep31252	journal	August 2016
Nano- and micro-sized honeycomb patterns through hierarchical self-assembly of metal-loaded diblock copolymer vesicles Pietsch, Torsten; Gindy, Nabil; Fahmi, Amir Soft Matter, Vol. 5, Issue 11 https://doi.org/10.1039/B814061H	journal	January 2009
Mesophyll conductance: the leaf corridors for photosynthesis Gago, Jorge; Daloso, Danilo M.; Carriquí, Marc Biochemical Society Transactions, Vol. 48, Issue 2 https://doi.org/10.1042/BST20190312	journal	March 2020
A three-dimensional model of CO2 transport in airspaces and mesophyll cells of a silver birch leaf Aalto, T.; Juurola, E. Plant, Cell and Environment, Vol. 25, Issue 11 https://doi.org/10.1046/j.0016-8025.2002.00906.x	journal	November 2002
Photosynthetic Responses of a Temperate Liana to Xylella fastidiosa Infection and Water Stress: Photosynthetic Responses of a Temperate Liana McElrone, A. J.; Forseth, I. N. Journal of Phytopathology, Vol. 152, Issue 1 https://doi.org/10.1046/j.1439-0434.2003.00794.x	journal	January 2004
Survival and growth of seedlings of 12 Chilean rainforest trees in two light environments: Gas exchange and biomass distribution correlates Lusk, Christopher H.; Del Pozo, Alejandro Austral Ecology, Vol. 27, Issue 2 https://doi.org/10.1046/j.1442-9993.2002.01168.x	journal	April 2002
Growth and photosynthetic down-regulation in Coffea arabica in response to restricted root volume Ronchi, Cláudio P.; DaMatta, Fábio M.; Batista, Karine D. Functional Plant Biology, Vol. 33, Issue 11 https://doi.org/10.1071/FP06147	journal	January 2006
The evolution and functional significance of leaf shape in the angiosperms Nicotra, Adrienne B.; Leigh, Andrea; Boyce, C. Kevin Functional Plant Biology, Vol. 38, Issue 7 https://doi.org/10.1071/FP11057	journal	January 2011
When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes Nardini, Andrea; Õunapuu-Pikas, Eele; Savi, Tadeja Functional Plant Biology, Vol. 41, Issue 9 https://doi.org/10.1071/FP13302	journal	January 2014
Photosynthetic Rate, Stomatal Conductance and Leaf Area in Two Cotton Species (Gossypium barbadense and Gossypium hirsutum) and their Relation with Heat Resistance and Yield Lu, Zhenmin; Chen, Jiwei; Percy, Richard G. Functional Plant Biology, Vol. 24, Issue 5 https://doi.org/10.1071/PP97056	journal	January 1997
Emergent patterns of growth controlled by multicellular form and mechanics Nelson, C. M.; Jean, R. P.; Tan, J. L. Proceedings of the National Academy of Sciences, Vol. 102, Issue 33 https://doi.org/10.1073/pnas.0502575102	journal	July 2005
Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading Amiard, V.; Mueh, K. E.; Demmig-Adams, B. Proceedings of the National Academy of Sciences, Vol. 102, Issue 36 https://doi.org/10.1073/pnas.0503784102	journal	August 2005
Cicatrization of Foliage Leaves II. Wound Responses of Certain Broad-Leaved Evergreens Wylie, Robert B. Botanical Gazette, Vol. 92, Issue 3 https://doi.org/10.1086/334197	journal	November 1931
The Ancestral Ecology of Angiosperms: Emerging Perspectives from Extant Basal Lineages Feild, Taylor S.; Arens, Nan Crystal; Dawson, Todd E. International Journal of Plant Sciences, Vol. 164, Issue S3 https://doi.org/10.1086/374193	journal	May 2003
The Evolution of Photosynthetic Anatomy in Viburnum (Adoxaceae) Chatelet, David S.; Clement, Wendy L.; Sack, Lawren International Journal of Plant Sciences, Vol. 174, Issue 9 https://doi.org/10.1086/673241	journal	November 2013
The Scaling of Genome Size and Cell Size Limits Maximum Rates of Photosynthesis with Implications for Ecological Strategies Roddy, Adam B.; Théroux-Rancourt, Guillaume; Abbo, Tito International Journal of Plant Sciences, Vol. 181, Issue 1 https://doi.org/10.1086/706186	journal	January 2020
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Phylocom: software for the analysis of phylogenetic community structure and trait evolution Webb, Campbell O.; Ackerly, David D.; Kembel, Steven W. Bioinformatics, Vol. 24, Issue 18 https://doi.org/10.1093/bioinformatics/btn358	journal	August 2008
Is Amphistomy an Adaptation to High Light? Optimality Models of Stomatal Traits along Light Gradients Muir, Christopher D. Integrative and Comparative Biology, Vol. 59, Issue 3 https://doi.org/10.1093/icb/icz085	journal	May 2019
Acclimation of photosynthesis to low temperature in Spinacia oleracea L. II. Effects of nitrogen supply Martindale, Wayne; Leegood, Richard C. Journal of Experimental Botany, Vol. 48, Issue 10 https://doi.org/10.1093/jxb/48.10.1873	journal	January 1997
Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression Nelson, E. A.; Sage, R. F. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/erm346	journal	June 2007
Live imaging of microtubule organization, cell expansion, and intercellular space formation in Arabidopsis leaf spongy mesophyll cells Zhang, Liyong; McEvoy, Delanie; Le, Yen The Plant Cell, Vol. 33, Issue 3 https://doi.org/10.1093/plcell/koaa036	journal	December 2020
Drought-induced photosynthetic inhibition and autumn recovery in two Mediterranean oak species (Quercus ilex and Quercus suber) Vaz, M.; Pereira, J. S.; Gazarini, L. C. Tree Physiology, Vol. 30, Issue 8 https://doi.org/10.1093/treephys/tpq044	journal	June 2010
Angiosperm leaf vein evolution was physiologically and environmentally transformative Boyce, C. Kevin; Brodribb, Tim J.; Feild, Taylor S. Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1663 https://doi.org/10.1098/rspb.2008.1919	journal	February 2009
Maximum CO ₂ diffusion inside leaves is limited by the scaling of cell size and genome size Théroux-Rancourt, Guillaume; Roddy, Adam B.; Earles, J. Mason Proceedings of the Royal Society B: Biological Sciences, Vol. 288, Issue 1945 https://doi.org/10.1098/rspb.2020.3145	journal	February 2021
Leaf Functional Anatomy in Relation to Photosynthesis Terashima, Ichiro; Hanba, Yuko T.; Tholen, Danny Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.165472	journal	November 2010
Beyond Porosity: 3D Leaf Intercellular Airspace Traits That Impact Mesophyll Conductance Earles, J. Mason; Theroux-Rancourt, Guillaume; Roddy, Adam B. Plant Physiology, Vol. 178, Issue 1 https://doi.org/10.1104/pp.18.00550	journal	July 2018
The Spatial Distribution of Chlorophyll in Leaves Borsuk, Aleca M.; Brodersen, Craig R. Plant Physiology, Vol. 180, Issue 3 https://doi.org/10.1104/pp.19.00094	journal	April 2019
A Direct Confirmation of the Standard Method of Estimating Intercellular Partial Pressure of CO ₂ Sharkey, Thomas D.; Imai, Katsu; Farquhar, Graham D. Plant Physiology, Vol. 69, Issue 3 https://doi.org/10.1104/pp.69.3.657	journal	March 1982
Intercellular Diffusion Limits to CO ₂ Uptake in Leaves : Studies in Air and Helox Parkhurst, David F.; Mott, Keith A. Plant Physiology, Vol. 94, Issue 3 https://doi.org/10.1104/pp.94.3.1024	journal	November 1990
Acclimation of leaf traits in seasonal light environments: Are non-native species more plastic? Martinez, Kelsey A.; Fridley, Jason D. Journal of Ecology, Vol. 106, Issue 5 https://doi.org/10.1111/1365-2745.12952	journal	March 2018
Does lateral gas diffusion in leaves matter? Morison, James I. L.; Lawson, Tracy Plant, Cell & Environment, Vol. 30, Issue 9 https://doi.org/10.1111/j.1365-3040.2007.01685.x	journal	September 2007
A new paradigm in leaf-level photosynthesis: direct and diffuse lights are not equal Brodersen, Craig R.; Vogelmann, Thomas C.; Williams, William E. Plant, Cell & Environment, Vol. 0, Issue 0 https://doi.org/10.1111/j.1365-3040.2007.01751.x	journal	November 2007
Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate: Photosynthetic temperature responses of Semillon Greer, Dennis H.; Weedon, Mark M. Plant, Cell & Environment, Vol. 35, Issue 6 https://doi.org/10.1111/j.1365-3040.2011.02471.x	journal	December 2011
Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification Brodribb, Tim J.; Feild, Taylor S. Ecology Letters, Vol. 13, Issue 2 https://doi.org/10.1111/j.1461-0248.2009.01410.x	journal	February 2010
Scaling and structure of dicotyledonous leaf venation networks: Leaf network geometry Price, Charles A.; Wing, Scott; Weitz, Joshua S. Ecology Letters, Vol. 15, Issue 2 https://doi.org/10.1111/j.1461-0248.2011.01712.x	journal	November 2011
Diffusion of CO2 and other gases inside leaves Parkhurst, David F. New Phytologist, Vol. 126, Issue 3 https://doi.org/10.1111/j.1469-8137.1994.tb04244.x	journal	March 1994
Xylem hydraulic and photosynthetic function of Gnetum (Gnetales) species from Papua New Guinea Feild, Taylor S.; Balun, Lawong New Phytologist, Vol. 177, Issue 3 https://doi.org/10.1111/j.1469-8137.2007.02306.x	journal	December 2007
Seeing the forest with the leaves - clues to canopy placement from leaf fossil size and venation characteristics Boyce, C. K. Geobiology, Vol. 7, Issue 2 https://doi.org/10.1111/j.1472-4669.2008.00176.x	journal	March 2009
Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms Feild, T. S.; Chatelet, D. S.; Brodribb, T. J. Geobiology, Vol. 7, Issue 2 https://doi.org/10.1111/j.1472-4669.2009.00189.x	journal	March 2009
smatr 3- an R package for estimation and inference about allometric lines: The smatr 3 - an R package Warton, David I.; Duursma, Remko A.; Falster, Daniel S. Methods in Ecology and Evolution, Vol. 3, Issue 2 https://doi.org/10.1111/j.2041-210X.2011.00153.x	journal	September 2011
Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future Sack, Lawren; Scoffoni, Christine New Phytologist, Vol. 198, Issue 4 https://doi.org/10.1111/nph.12253	journal	April 2013
A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity Magallón, Susana; Gómez‐Acevedo, Sandra; Sánchez‐Reyes, Luna L. New Phytologist, Vol. 207, Issue 2 https://doi.org/10.1111/nph.13264	journal	December 2014
Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves Fiorin, Lucia; Brodribb, Timothy J.; Anfodillo, Tommaso New Phytologist, Vol. 209, Issue 1 https://doi.org/10.1111/nph.13577	journal	July 2015
The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging Théroux-Rancourt, Guillaume; Earles, J. Mason; Gilbert, Matthew E. New Phytologist, Vol. 215, Issue 4 https://doi.org/10.1111/nph.14687	journal	July 2017
Cell and chloroplast anatomical features are poorly estimated from 2D cross‐sections Harwood, Richard; Goodman, Elinor; Gudmundsdottir, Marin New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16219	journal	November 2019
The Plant DNA C‐values database (release 7.1): an updated online repository of plant genome size data for comparative studies Pellicer, Jaume; Leitch, Ilia J. New Phytologist, Vol. 226, Issue 2 https://doi.org/10.1111/nph.16261	journal	November 2019
Three-dimensional microscale modelling of CO ₂ transport and light propagation in tomato leaves enlightens photosynthesis : 3-D modelling of photosynthesis in leaves Ho, Quang Tri; Berghuijs, Herman N. C.; Watté, Rodrigo Plant, Cell & Environment, Vol. 39, Issue 1 https://doi.org/10.1111/pce.12590	journal	July 2015
Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity Lehmeier, Christoph; Pajor, Radoslaw; Lundgren, Marjorie R. The Plant Journal, Vol. 92, Issue 6 https://doi.org/10.1111/tpj.13727	journal	November 2017
Spongy Mesophyll Remains in Fossil Leaf Compressions Chandrasekharam, A. Science, Vol. 177, Issue 4046 https://doi.org/10.1126/science.177.4046.354	journal	July 1972
Global climatic drivers of leaf size Wright, Ian J.; Dong, Ning; Maire, Vincent Science, Vol. 357, Issue 6354 https://doi.org/10.1126/science.aal4760	journal	August 2017
BoneJ2 - refactoring established research software Domander, Richard; Felder, Alessandro A.; Doube, Michael Wellcome Open Research, Vol. 6 https://doi.org/10.12688/wellcomeopenres.16619.1	journal	January 2021
Three-dimensional radiation transfer modeling in a dicotyledon leaf Govaerts, Yves M.; Jacquemoud, Stéphane; Verstraete, Michel M. Applied Optics, Vol. 35, Issue 33 https://doi.org/10.1364/AO.35.006585	journal	January 1996
Genome downsizing, physiological novelty, and the global dominance of flowering plants Simonin, Kevin A.; Roddy, Adam B. PLOS Biology, Vol. 16, Issue 1 https://doi.org/10.1371/journal.pbio.2003706	journal	January 2018
Phylogeny and Divergence Times of Gymnosperms Inferred from Single-Copy Nuclear Genes Lu, Ying; Ran, Jin-Hua; Guo, Dong-Mei PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0107679	journal	September 2014
Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants Boyce, C. Kevin; Knoll, Andrew H. Paleobiology, Vol. 28, Issue 1 https://doi.org/10.1666/0094-8373(2002)028<0070:EODPAT>2.0.CO;2	journal	January 2002
Scaling mass and Morphology in Leaves: an Extension of the wbe Model Price, Charles A.; Enquist, Brian J. Ecology, Vol. 88, Issue 5 https://doi.org/10.1890/06-1158	journal	May 2007
Net Photosynthesis and Growth of Three Novel Woody Species Under Water Stress: Calycanthus occidentalis, Fraxinus anomala, and Pinckneya pubens Stewart, J. Ryan; Landes, Reid D.; Koeser, Andrew K. HortScience, Vol. 42, Issue 6 https://doi.org/10.21273/HORTSCI.42.6.1341	journal	October 2007
Influence of Spring and Fall Drought Stresses on Growth and Gas Exchange during Stress and Posttransplant of Container-grown Magnoli ×soulangiana `Jane' Fernandez, R. Thomas; Schutzki, Robert E.; Prevete, Kelly J. Journal of the American Society for Horticultural Science, Vol. 127, Issue 1 https://doi.org/10.21273/JASHS.127.1.38	journal	January 2002
Photosynthetic Responses of Container-grown Illicium L. Taxa to Sun and Shade Olsen, Richard T.; Ruter, John M.; Rieger, Mark W. Journal of the American Society for Horticultural Science, Vol. 127, Issue 6 https://doi.org/10.21273/JASHS.127.6.919	journal	November 2002
Carbon Assimilation and Carbohydrate Metabolism of `Concord' Grape (Vitis labrusca L.) Leaves in Response to Nitrogen Supply Chen, Li-Song; Cheng, Lailiang Journal of the American Society for Horticultural Science, Vol. 128, Issue 5 https://doi.org/10.21273/JASHS.128.5.0754	journal	September 2003
Leaf Form and Photosynthesis Smith, William K.; Vogelmann, Thomas C.; DeLucia, Evan H. BioScience, Vol. 47, Issue 11 https://doi.org/10.2307/1313100	journal	December 1997
Angiosperm leaf vein patterns are linked to leaf functions in a global-scale data set Walls, Ramona L. American Journal of Botany, Vol. 98, Issue 2 https://doi.org/10.3732/ajb.1000154	journal	February 2011

Similar Records

Localized growth and remodelling drives spongy mesophyll morphogenesis

Journal Article · 2022 · Interface (Online) · OSTI ID:2422698

Treado, John D.; Roddy, Adam B.; Théroux-Rancourt, Guillaume; +5 more

The reduction in leaf area precedes that in photosynthesis under potassium deficiency: the importance of leaf anatomy

Journal Article · 2020 · New Phytologist · OSTI ID:1632250

Hu, Wenshi; Lu, Zhifeng; Meng, Fanjin; +5 more

The bias of a two‐dimensional view: comparing two‐dimensional and three‐dimensional mesophyll surface area estimates using noninvasive imaging

Journal Article · 2017 · New Phytologist · OSTI ID:1373818

Théroux‐Rancourt, Guillaume; Earles, J. Mason; Gilbert, Matthew E.; +4 more

Title: Structural organization of the spongy mesophyll

Citation Formats

References (85)

Similar Records

Related Subjects